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Functional Characterization of Arabidopsis thaliana WRKY39 in ...

Functional Characterization of Arabidopsis thaliana WRKY39 in ...

Functional Characterization of Arabidopsis thaliana WRKY39 in

Mol. Cells 29, 475-483, May 31, 2010 DOI/10.1007/s10059-010-0059-2 Functional Characterization of Arabidopsis thaliana WRKY39 in Heat Stress Shujia Li 1,2 , Xiang Zhou 2 , Ligang Chen 2 , Weidong Huang 1, *, and Diqiu Yu 2, * Arabidopsis thaliana WRKY39, a transcription factor that is induced by heat stress, is a member of the group II WRKY proteins and responds to both abiotic and biotic stress. Heat-treated seeds and plants of WRKY39 knock-down mutants had increased susceptibility to heat stress, showing reduced germination, decreased survival, and elevated electrolyte leakage compared with wild-type plants. In contrast, WRKY39 over-expressing plants exhibited enhanced thermotolerance compared with wild-type plants. RT-PCR and qRT-PCR analysis of wrky39 mutants and WRKY39 over-expressing plants identified putative genes regulated by WRKY39. Consistent with a role for WRKY39 in heat tolerance, the expression levels of salicylic acid (SA)regulated PR1 and SA-related MBF1c genes were downregulated in wrky39 mutants. In contrast, over-expression of WRKY39 increased the expression of PR1 and MBF1c. The WRKY39 transcript was induced in response to treatment with SA or methyljasmonate. Analysis of heat stressinduced WRKY39 in defense signaling mutants, including coi1, ein2, and sid2, further indicated that WRKY39 was positively co-regulated by the SA and jasmonate (JA) signaling pathways. Together, these findings reveal that heat stress-induced WRKY39 positively regulates the cooperation between the SA- and JA-activated signaling pathways that mediate responses to heat stress. INTRODUCTION Extreme temperature is an adverse environmental stress that severely impairs plant growth and development (Guy, 1999). Plants have a natural capacity to ameliorate the effects of heat shock (HS) (Hong and Vierling, 2000). Previous studies have shown that HS transcription factors (Hsfs) play an important role in thermotolerance in plants and other organisms by regulating HS proteins (Hsps) (Baniwal et al., 2004; Mishra et al., 2002; Panchuk et al., 2002; von Koskull-Döring et al., 2007). However, plants with mutations disrupting abscisic acid (ABA), salicylic acid (SA), hydrogen peroxide, ethylene (ET), or calcium signaling, which appear to accumulate similar Hsp101 and other Hsps to wild-type plants, displayed thermosensitivity (Larkindale and Huang, 2005; Larkindale et al., 2005). Exoge- Galley Proof Molecules and Cells ©2010 KSMCB nous application of these signaling agents to plants can also result in a degree of enhanced thermotolerance without an accompanying accumulation of Hsps (Larkindale and Knight, 2002). Thus, thermotolerance is affected by a complex network of changes in plants, only one of which is the production of Hsps (Larkindale and Vierling, 2008). The SA-mediated pathway has been reported to protect potato, mustard, tobacco, tomato, bean, and Arabidopsis thaliana from heat stress (Dat et al., 1998; 2000; Larkindale and Knight, 2002; Lopez-Delgado et al., 1998; Senaratna et al., 2000). HS was found to induce SA-regulated pathogenesis-related 1 (PR1) transcripts, and the constitutive expression of PR1 protein mutant (cpr1-5) exhibited an enhanced thermotolerant phenotype (Clarke et al., 2004; 2009). This indicates that SA and PR1, originally defined as being involved in antipathogenic responses, can also promote heat tolerance in A. thaliana. The earlier study revealed that multiple bridging factor 1c (MBF1c) is a key regulator of thermotolerance in A. thaliana that functions upstream of SA and PR1 during heat stress. In addition, MBF1c-mediated thermotolerance is independent of Hsps expression (Suzuki et al., 2008). Jasmonate (JA) has been implicated in signaling in response to both biotic and abiotic stresses (Balbi and Devoto, 2008; Wasternack, 2006; 2007). Wounding and pathogen infection, or exposure to ozone, cause endogenous JA accumulation (Howe, 2004; Kanna et al., 2003; Rao et al., 2000; Vijayan, et al., 1998; Wasternack, 2006). Heat stress also induces the JA signal transduction pathway (Clarke et al., 2009). The relationship between JA- and SA- signaling has often been shown to be antagonistic. In A. thaliana, pathogen-induced SA accumulation is associated with the suppression of JA signaling (Spoel et al., 2003). In contrast, a recent finding has demonstrated that JA acts with SA to confer thermotolerance in A. thaliana, and that Hsps apparently play no role in JA-conferred thermotolerance in this species (Clarke et al., 2009). The WRKY transcription factor superfamily has been suggested to have a key role in biotic and abiotic stress (Eulgem and Somssich, 2007; Miller et al., 2008). The A. thaliana WRKY superfamily consists of over 74 members, and is sub-divided into three groups on the basis of the number of WRKY (WRKYGQK) domains and the features of their zinc finger-like motif (Eulgem et al., 2000). Earlier reports have demonstrated 1 2 College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China *Correspondence: huanggwd@263.net (WH); ydq@xtbg.ac.cn (DY) Received November 13, 2009; revised January 13, 2010; accepted January 19, 2010; published online April 12, 2010 Keywords: heat stress, jasmonate, salicylic acid, thermotolerance, WRKY39 transcription factor

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